Structure of human chromatin-remodelling PBAF complex bound to a nucleosome

  • Luger, K., Mader, A. W., Richmond, R. K., Sargent, D. F. & Richmond, T. J. Crystal structure of the nucleosome core particle at 2.8 angstrom resolution. Nature 389, 251–260 (1997).

    CAS   PubMed  Article  ADS  Google Scholar 

  • Clapier, C. R. & Cairns, B. R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 78, 273–304 (2009).

    CAS  PubMed  Article  Google Scholar 

  • Yan, L. & Chen, Z. A unifying mechanism of DNA translocation underlying chromatin remodeling. Trends Biochem. Sci. 45, 217–227 (2020).

    CAS  PubMed  Article  Google Scholar 

  • Alfert, A., Moreno, N. & Kerl, K. The BAF complex in development and disease. Epigenetics Chromatin 12, 19 (2019).

    PubMed  PubMed Central  Article  Google Scholar 

  • Kwon, H., Imbalzano, A. N., Khavari, P. A., Kingston, R. E. & Green, M. R. Nucleosome disruption and enhancement of activator binding by a human SW1/SNF complex. Nature 370, 477–481 (1994).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Wang, W. et al. Purification and biochemical heterogeneity of the mammalian SWI–SNF complex. EMBO J. 15, 5370–5382 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sokpor, G., Xie, Y., Rosenbusch, J. & Tuoc, T. Chromatin remodeling BAF (SWI/SNF) complexes in neural development and disorders. Front. Mol. Neurosci. 10, 243 (2017).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Hodges, C., Kirkland, J. G. & Crabtree, G. R. The many roles of BAF (mSWI/SNF) and PBAF complexes in cancer. Cold Spring Harb. Perspect Med. 6, a026930 (2016).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  • Mittal, P. & Roberts, C. W. M. The SWI/SNF complex in cancer—biology, biomarkers and therapy. Nat. Rev. Clin. Oncol. 17, 435–448 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sundaramoorthy, R. & Owen-Hughes, T. Chromatin remodelling comes into focus. F1000Res 9, https://doi.org/10.12688/f1000research.21933.1 (2020).

  • Pan, J. et al. The ATPase module of mammalian SWI/SNF family complexes mediates subcomplex identity and catalytic activity-independent genomic targeting. Nat. Genet. 51, 618–626 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Nakayama, R. T. et al. SMARCB1 is required for widespread BAF complex-mediated activation of enhancers and bivalent promoters. Nat. Genet. 49, 1613–1623 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Lemon, B., Inouye, C., King, D. S. & Tjian, R. Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 414, 924–928 (2001).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Miao, D. et al. Genomic correlates of response to immune checkpoint therapies in clear cell renal cell carcinoma. Science 359, 801–806 (2018).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Pan, D. et al. A major chromatin regulator determines resistance of tumor cells to T cell-mediated killing. Science 359, 770–775 (2018).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Ho, P. J., Lloyd, S. M. & Bao, X. Unwinding chromatin at the right places: how BAF is targeted to specific genomic locations during development. Development 146, dev178780 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Leschziner, A. E., Lemon, B., Tjian, R. & Nogales, E. Structural studies of the human PBAF chromatin-remodeling complex. Structure 13, 267–275 (2005).

    CAS  PubMed  Article  Google Scholar 

  • Mashtalir, N. et al. A structural model of the endogenous human BAF complex informs disease mechanisms. Cell 183, 802–817.e824 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • He, S. et al. Structure of nucleosome-bound human BAF complex. Science 367, 875–881 (2020).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Mashtalir, N. et al. Modular organization and assembly of SWI/SNF family chromatin remodeling complexes. Cell 175, 1272–1288.e1220 (2018).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Patsialou, A., Wilsker, D. & Moran, E. DNA-binding properties of ARID family proteins. Nucleic Acids Res. 33, 66–80 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Charlop-Powers, Z., Zeng, L., Zhang, Q. & Zhou, M. M. Structural insights into selective histone H3 recognition by the human Polybromo bromodomain 2. Cell Res. 20, 529–538 (2010).

    CAS  PubMed  Article  Google Scholar 

  • Sun, H. et al. Solution structure of BRD7 bromodomain and its interaction with acetylated peptides from histone H3 and H4. Biochem. Biophys. Res. Commun. 358, 435–441 (2007).

    CAS  PubMed  Article  Google Scholar 

  • Valencia, A. M. et al. Recurrent SMARCB1 mutations reveal a nucleosome acidic patch interaction site that potentiates mSWI/SNF complex chromatin remodeling. Cell 179, 1342–1356.e1323 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Ye, Y. et al. Structure of the RSC complex bound to the nucleosome. Science 366, 838–843 (2019).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • He, Z., Chen, K., Ye, Y. & Chen, Z. Structure of the SWI/SNF complex bound to the nucleosome and insights into the functional modularity. Cell Discov. 7, 28 (2021).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Wagner, F. R. et al. Structure of SWI/SNF chromatin remodeller RSC bound to a nucleosome. Nature 579, 448–451 (2020).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Han, Y., Reyes, A. A., Malik, S. & He, Y. Cryo-EM structure of SWI/SNF complex bound to a nucleosome. Nature 579, 452–455 (2020).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Cerami, E. et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2, 401–404 (2012).

    PubMed  Article  Google Scholar 

  • Yan, L., Wang, L., Tian, Y., Xia, X. & Chen, Z. Structure and regulation of the chromatin remodeller ISWI. Nature 540, 466–469 (2016).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Liu, X., Li, M., Xia, X., Li, X. & Chen, Z. Mechanism of chromatin remodelling revealed by the Snf2-nucleosome structure. Nature 544, 440–445 (2017).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Yan, L., Wu, H., Li, X., Gao, N. & Chen, Z. Structures of the ISWI–nucleosome complex reveal a conserved mechanism of chromatin remodeling. Nat. Struct. Mol. Biol. 26, 258–266 (2019).

    CAS  PubMed  Article  Google Scholar 

  • Li, M. et al. Mechanism of DNA translocation underlying chromatin remodelling by Snf2. Nature 567, 409–413 (2019).

    CAS  PubMed  Article  ADS  Google Scholar 

  • Hodges, H. C. et al. Dominant-negative SMARCA4 mutants alter the accessibility landscape of tissue-unrestricted enhancers. Nat. Struct. Mol. Biol. 25, 61–72 (2018).

    CAS  PubMed  Article  Google Scholar 

  • Dykhuizen, E. C. et al. BAF complexes facilitate decatenation of DNA by topoisomerase IIα. Nature 497, 624–627 (2013).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Sen, P., Ghosh, S., Pugh, B. F. & Bartholomew, B. A new, highly conserved domain in Swi2/Snf2 is required for SWI/SNF remodeling. Nucleic Acids Res. 39, 9155–9166 (2011).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Sen, P. et al. The SnAC domain of SWI/SNF is a histone anchor required for remodeling. Mol. Cell. Biol. 33, 360–370 (2013).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Baker, R. W. et al. Structural insights into assembly and function of the RSC chromatin remodeling complex. Nat. Struct. Mol. Biol. 28, 71–80 (2021).

    CAS  PubMed  Article  Google Scholar 

  • McGinty, R. K. & Tan, S. Principles of nucleosome recognition by chromatin factors and enzymes. Curr. Opin. Struct. Biol. 71, 16–26 (2021).

    CAS  PubMed  Article  Google Scholar 

  • Wang, L., Chen, K. & Chen, Z. Structural basis of ALC1/CHD1L autoinhibition and the mechanism of activation by the nucleosome. Nat. Commun. 12, 4057 (2021).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Gamarra, N., Johnson, S. L., Trnka, M. J., Burlingame, A. L. & Narlikar, G. J. The nucleosomal acidic patch relieves auto-inhibition by the ISWI remodeler SNF2h. eLife 7, e35322 (2018).

    PubMed  PubMed Central  Article  Google Scholar 

  • Bacic, L. et al. Structure and dynamics of the chromatin remodeler ALC1 bound to a PARylated nucleosome. eLife 10, e71420 (2021).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Dao, H. T., Dul, B. E., Dann, G. P., Liszczak, G. P. & Muir, T. W. A basic motif anchoring ISWI to nucleosome acidic patch regulates nucleosome spacing. Nat. Chem. Biol. 16, 134–142 (2020).

    CAS  PubMed  Article  Google Scholar 

  • Emery, P., Durand, B., Mach, B. & Reith, W. RFX proteins, a novel family of DNA binding proteins conserved in the eukaryotic kingdom. Nucleic Acids Res. 24, 803–807 (1996).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Jiang, H. et al. Chromatin remodeling factor ARID2 suppresses hepatocellular carcinoma metastasis via DNMT1–Snail axis. Proc. Natl Acad. Sci. USA 117, 4770–4780 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Varela, I. et al. Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469, 539–542 (2011).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Gao, W., Li, W., Xiao, T., Liu, X. S. & Kaelin, W. G. Jr Inactivation of the PBRM1 tumor suppressor gene amplifies the HIF-response in VHL−/− clear cell renal carcinoma. Proc. Natl Acad. Sci. USA 114, 1027–1032 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Allen, M. D., Freund, S. M., Zinzalla, G. & Bycroft, M. The SWI/SNF subunit INI1 contains an N-terminal winged helix DNA binding domain that is a target for mutations in schwannomatosis. Structure 23, 1344–1349 (2015).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Chabanon, R. M., Morel, D. & Postel-Vinay, S. Exploiting epigenetic vulnerabilities in solid tumors: novel therapeutic opportunities in the treatment of SWI/SNF-defective cancers. Semin. Cancer Biol. 61, 180–198 (2020).

    CAS  PubMed  Article  Google Scholar 

  • Barisic, D., Stadler, M. B., Iurlaro, M. & Schubeler, D. Mammalian ISWI and SWI/SNF selectively mediate binding of distinct transcription factors. Nature 569, 136–140 (2019).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

  • Luger, K., Rechsteiner, T. J. & Richmond, T. J. Expression and purification of recombinant histones and nucleosome reconstitution. Methods Mol. Biol. https://doi.org/10.1385/1-59259-681-9:1 (1999).

  • Dyer, P. N. et al. Reconstitution of nucleosome core particles from recombinant histones and DNA. Methods Enzymol. 375, 23–44 (2004).

    CAS  PubMed  Article  Google Scholar 

  • Chen, Z. L. et al. A high-speed search engine pLink 2 with systematic evaluation for proteome-scale identification of cross-linked peptides. Nat. Commun. 10, 3404 (2019).

    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

  • Lei, J. & Frank, J. Automated acquisition of cryo-electron micrographs for single particle reconstruction on an FEI Tecnai electron microscope. J. Struct. Biol. 150, 69–80 (2005).

    PubMed  Article  Google Scholar 

  • Scheres, S. H. RELION: implementation of a Bayesian approach to cryo-EM structure determination. J. Struct. Biol. 180, 519–530 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Rohou, A. & Grigorieff, N. CTFFIND4: fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).

    PubMed  PubMed Central  Article  Google Scholar 

  • Wang, N. et al. Structural basis of human monocarboxylate transporter 1 inhibition by anti-cancer drug candidates. Cell 184, 370–383.e313 (2021).

    CAS  PubMed  Article  Google Scholar 

  • Pettersen, E. F. et al. UCSF Chimera—a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).

    CAS  PubMed  Article  Google Scholar 

  • Patel, A. B. et al. Architecture of the chromatin remodeler RSC and insights into its nucleosome engagement. eLife 8, e54449 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Bastiray, A., Giri, M. & Singh, M. Sequential backbone resonance assignment of AT-rich interaction domain of human BAF200. Biomol. NMR Assign. 13, 115–119 (2019).

    CAS  PubMed  Article  Google Scholar 

  • Du, Z. et al. The trRosetta server for fast and accurate protein structure prediction. Nat. Protoc. 16, 5634–5651 (2021).

    CAS  PubMed  Article  Google Scholar 

  • Zhou, N., Wang, H. & Wang, J. EMBuilder: a template matching-based automatic model-building program for high-resolution cryo-electron microscopy maps. Sci Rep. 7, 2664 (2017).

    PubMed  PubMed Central  Article  ADS  CAS  Google Scholar 

  • Afonine, P. V. et al. Towards automated crystallographic structure refinement with phenix.refine. Acta Crystallogr. D 68, 352–367 (2012).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  • Makde, R. D., England, J. R., Yennawar, H. P. & Tan, S. Structure of RCC1 chromatin factor bound to the nucleosome core particle. Nature 467, 562–566 (2010).

    CAS  PubMed  PubMed Central  Article  ADS  Google Scholar 

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